How do "mute" cicadas produce their calling songs?

Abstract

Insects have evolved a variety of structures and mechanisms to produce sounds, which are used for communication both within and between species. Among acoustic insects, cicada males are particularly known for their loud and diverse sounds which function importantly in communication. The main method of sound production in cicadas is the tymbal mechanism, and a relative small number of cicada species possess both tymbal and stridulatory organs. However, cicadas of the genus Karenia do not have any specialized sound-producing structures, so they are referred to as "mute". This denomination is quite misleading, as they indeed produce sounds. Here, we investigate the sound-producing mechanism and acoustic communication of the "mute" cicada, Karenia caelatata, and discover a new sound-production mechanism for cicadas: i.e., K. caelatata produces impact sounds by banging the forewing costa against the operculum. The temporal, frequency and amplitude characteristics of the impact sounds are described. Morphological studies and reflectance-based analyses reveal that the structures involved in sound production of K. caelatata (i.e., forewing, operculum, cruciform elevation, and wing-holding groove on scutellum) are all morphologically modified. Acoustic playback experiments and behavioral observations suggest that the impact sounds of K. caelatata are used in intraspecific communication and function as calling songs. The new sound-production mechanism expands our knowledge on the diversity of acoustic signaling behavior in cicadas and further underscores the need for more bioacoustic studies on cicadas which lack tymbal mechanism.

Fig 1. Costa-ablation experiment.

(a) A male with wings spreaded to show the forewing costa. (b) A male with wings spreaded to show the forewing costa removed.

Fig 2. Forewing costas and average reflectance profiles of the 12 species included in this study.

(a) Average reflectance profiles. Scale bar for all panels in (a) = 1 cm. (b) Average reflectance profiles. The dots in (b) denote the 23 location of the spectral bands selected for the classification of difference between non-mute and mute cicadas.

Fig 3. The sound-producing structures of K. caelatata.

(a, b, c) Ventral, dorsal, and lateral view of a male with red box indicating the operculum involved in sound production. (d) Right red arrow marks the wing-holding groove of a male with right wing spread; left red arrow indicates that the basal posterior margin of the forewing is fixed in the wing-holding groove. (e) The forewing costa is supported over the operculum (red arrow).

Fig 4. Oscillograms of sounds recorded from male K. caelatata after ablation of the costas of forewings.

(a) Oscillogram of three sounds produced by a post-ablated male. (b) Detailed oscillogram of a single sound produced by a post-ablated male.

Fig 5. Forewing and body length of the 12 species included in this study.

(a) Forewing length. (b) Body length. (c) Forewing/body ratio. Different letters represent significant difference at the 0.05-level.

Fig 6. Analysis of sounds produced by male K. caelatata.

(a) Oscillogram of three impact sounds produced by a male. (b, c) Oscillogram and spectrogram of an impact sound. (d) Detailed oscillogram of an impact sound.